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PMID: 8816814 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

c-myc activation renders proliferation of Epstein-Barr virus (EBV)-transformed cells independent of EBV nuclear antigen 2 and latent membrane protein 1.

Polack A, Hörtnagel K, Pajic A, Christoph B, Baier B, Falk M, Mautner J, Geltinger C, Bornkamm GW, Kempkes B

Abstract

Two genetic events contribute to the development of endemic Burkitt lymphoma (BL) infection of B lymphocytes with Epstein-Barr virus (EBV) and the activation of the protooncogene c-myc through chromosomal translocation. The viral genes EBV nuclear antigen 2 (EBNA2) and latent membrane protein 1 (LMP1) are essential for transformation of primary human B cells by EBV in vitro; however, these genes are not expressed in BL cells in vivo. To address the question whether c-myc activation might abrogate the requirement of the EBNA2 and LMP1 function, we have introduced an activated c-myc gene into an EBV-transformed cell line in which EBNA2 was rendered estrogen-dependent through fusion with the hormone binding domain of the estrogen receptor. The c-myc gene was placed under the control of regulatory elements of the immunoglobulin kappa locus composed a matrix attachment region, the intron enhancer, and the 3' enhancer. We show here that transfection of a c-myc expression plasmid followed by selection for high MYC expression is capable of inducing continuous proliferation of these cells in the absence of functional EBNA2 and LMP1. c-myc-induced hormone-independent proliferation was associated with a dramatic change in the growth behavior as well as cell surface marker expression of these cells. The typical lymphoblastoid morphology and phenotype of EBV-transformed cells completely changed into that of BL cells in vivo. We conclude that the phenotype of BL cells reflects the expression pattern of viral and cellular genes rather than its germinal center origin.

MeSH Terms
Antigens, CD/biosynthesis Burkitt Lymphoma Cell Division Cell Line, Transformed Epstein-Barr Virus Nuclear Antigens/biosynthesis Estrogens/pharmacology Flow Cytometry Gene Expression Regulation, Viral Genes, myc Herpesvirus 4, Human/genetics,physiology Humans Proto-Oncogene Proteins c-myc/biosynthesis Receptors, Estrogen/biosynthesis Recombinant Fusion Proteins/biosynthesis Trans-Activators/biosynthesis Transfection Viral Matrix Proteins/biosynthesis
Chemicals
Antigens, CD EBV-associated membrane antigen, Epstein-Barr virus Epstein-Barr Virus Nuclear Antigens Estrogens Proto-Oncogene Proteins c-myc Receptors, Estrogen Recombinant Fusion Proteins Trans-Activators Viral Matrix Proteins
Authors & Affiliations
10 authors, click to expand affiliations / ORCID
Polack A
Institut für Klinische Molekularbiologic und Tumorgenetik, GSF-Forschungszentrum für Umwelt und Gesundheit, Munich, Germany. [email protected]
Hörtnagel K
Pajic A
Christoph B
Baier B
Falk M
Mautner J
Geltinger C
Bornkamm G W
Kempkes B
References (51)
51 references, click to expand
  1. Specific chromosomal translocations and the genesis of B-cell-derived tumors in mice and men.
    Cell. 1983 Feb;32(2):311-5 PMID: 6402307
  2. Stable replication of plasmids derived from Epstein-Barr virus in various mammalian cells.
    Nature. 1985 Feb 28-Mar 6;313(6005):812-5 PMID: 2983224
  3. Epstein-Barr virus latent gene expression during the initiation of B cell immortalization.
    J Gen Virol. 1989 Jul;70 ( Pt 7):1755-64 PMID: 2544663
  4. Genetic analysis of immortalizing functions of Epstein-Barr virus in human B lymphocytes.
    Nature. 1989 Aug 3;340(6232):393-7 PMID: 2547164
  5. Chromosomal translocation t(1;19) results in synthesis of a homeobox fusion mRNA that codes for a potential chimeric transcription factor.
    Cell. 1990 Feb 23;60(4):535-45 PMID: 1967982
  6. A new homeobox gene contributes the DNA binding domain of the t(1;19) translocation protein in pre-B ALL.
    Cell. 1990 Feb 23;60(4):547-55 PMID: 1967983
  7. Stable transfection of Epstein-Barr virus (EBV) nuclear antigen 2 in lymphoma cells containing the EBV P3HR1 genome induces expression of B-cell activation molecules CD21 and CD23.
    J Virol. 1990 Mar;64(3):1002-13 PMID: 2154588
  8. Epstein-Barr virus nuclear antigen 2 induces expression of the virus-encoded latent membrane protein.
    J Virol. 1990 May;64(5):2126-34 PMID: 2157875
  9. The level of c-fgr RNA is increased by EBNA-2, an Epstein-Barr virus gene required for B-cell immortalization.
    J Virol. 1990 Jun;64(6):2530-6 PMID: 2159528
  10. Epstein-Barr virus-encoded nuclear antigen 2 activates the viral latent membrane protein promoter by modulating the activity of a negative regulatory element.
    Proc Natl Acad Sci U S A. 1990 Oct;87(19):7390-4 PMID: 2170976
  11. Down-regulation of LFA-1 adhesion receptors by C-myc oncogene in human B lymphoblastoid cells.
    Science. 1990 Nov 2;250(4981):682-6 PMID: 2237417
  12. Sequence-specific DNA binding by the c-Myc protein.
    Science. 1990 Nov 23;250(4984):1149-51 PMID: 2251503
  13. Epstein-Barr virus nuclear antigen 2 activates transcription of the terminal protein gene.
    J Virol. 1991 Jan;65(1):415-23 PMID: 1845900
  14. Recombinant Epstein-Barr virus with small RNA (EBER) genes deleted transforms lymphocytes and replicates in vitro.
    Proc Natl Acad Sci U S A. 1991 Feb 15;88(4):1546-50 PMID: 1847527
  15. EBNA-2 transactivates a lymphoid-specific enhancer in the BamHI C promoter of Epstein-Barr virus.
    J Virol. 1991 May;65(5):2164-9 PMID: 1850003
  16. Role for the Epstein-Barr virus nuclear antigen 2 in viral promoter switching during initial stages of infection.
    Proc Natl Acad Sci U S A. 1991 May 1;88(9):3942-6 PMID: 1850841
  17. Induction of bcl-2 expression by Epstein-Barr virus latent membrane protein 1 protects infected B cells from programmed cell death.
    Cell. 1991 Jun 28;65(7):1107-15 PMID: 1648447
  18. Host cell and EBNA-2 regulation of Epstein-Barr virus latent-cycle promoter activity in B lymphocytes.
    J Virol. 1992 Jan;66(1):496-504 PMID: 1309259
  19. Use of second-site homologous recombination to demonstrate that Epstein-Barr virus nuclear protein 3B is not important for lymphocyte infection or growth transformation in vitro.
    J Virol. 1992 May;66(5):2893-903 PMID: 1313908
  20. The t(4;11) chromosome translocation of human acute leukemias fuses the ALL-1 gene, related to Drosophila trithorax, to the AF-4 gene.
    Cell. 1992 Nov 13;71(4):701-8 PMID: 1423625
  21. An EBV membrane protein expressed in immortalized lymphocytes transforms established rodent cells.
    Cell. 1985 Dec;43(3 Pt 2):831-40 PMID: 3000618
  22. Pathogenesis of Burkitt lymphoma: expression of an activated c-myc oncogene causes the tumorigenic conversion of EBV-infected human B lymphoblasts.
    Cell. 1987 Apr 24;49(2):161-70 PMID: 3032447
  23. N segment insertion and region-directed somatic hypermutation in a kappa gene of a t(2;8) chromosomal translocation.
    Nucleic Acids Res. 1987 Jun 25;15(12):4877-88 PMID: 3110741
  24. Differences in B cell growth phenotype reflect novel patterns of Epstein-Barr virus latent gene expression in Burkitt's lymphoma cells.
    EMBO J. 1987 Sep;6(9):2743-51 PMID: 2824192
  25. Truncation does not abrogate transcriptional downregulation of the c-myc gene by sodium butyrate in Burkitt's lymphoma cells.
    EMBO J. 1987 Oct;6(10):2959-64 PMID: 3691477
  26. Relationship between myc oncogene activation and MHC class I expression.
    Adv Cancer Res. 1993;60:181-246 PMID: 8417500
  27. The Epstein-Barr virus nuclear antigen 2 interacts with an EBNA2 responsive cis-element of the terminal protein 1 gene promoter.
    EMBO J. 1993 Jan;12(1):167-75 PMID: 8381349
  28. A trithorax-like gene is interrupted by chromosome 11q23 translocations in acute leukaemias.
    Nat Genet. 1992 Oct;2(2):113-8 PMID: 1303259
  29. Deletion of DNA encoding the first five transmembrane domains of Epstein-Barr virus latent membrane proteins 2A and 2B.
    J Virol. 1993 Aug;67(8):5068-74 PMID: 8392630
  30. Latent membrane protein of Epstein-Barr virus induces cellular phenotypes independently of expression of Bcl-2.
    J Virol. 1993 Sep;67(9):5269-78 PMID: 8394449
  31. Regulatory elements in the immunoglobulin kappa locus induce c-myc activation and the promoter shift in Burkitt's lymphoma cells.
    EMBO J. 1993 Oct;12(10):3913-20 PMID: 8404859
  32. Epstein-Barr virus latent membrane protein 1 is essential for B-lymphocyte growth transformation.
    Proc Natl Acad Sci U S A. 1993 Oct 1;90(19):9150-4 PMID: 8415670
  33. Epstein-Barr virus strategy in normal and neoplastic B cells.
    Cell. 1994 Jun 17;77(6):791-3 PMID: 8004668
  34. Upregulation of bcl-2 by the Epstein-Barr virus latent membrane protein LMP1: a B-cell-specific response that is delayed relative to NF-kappa B activation and to induction of cell surface markers.
    J Virol. 1994 Sep;68(9):5602-12 PMID: 7520093
  35. Epstein-Barr virus latency in blood mononuclear cells: analysis of viral gene transcription during primary infection and in the carrier state.
    J Virol. 1994 Nov;68(11):7374-85 PMID: 7933121
  36. Monoclonal antibodies directed against the Epstein-Barr virus-encoded nuclear antigen 1 (EBNA1): immunohistologic detection of EBNA1 in the malignant cells of Hodgkin's disease.
    Blood. 1994 Dec 1;84(11):3792-8 PMID: 7949135
  37. Epstein-Barr virus nuclear antigen 2 exerts its transactivating function through interaction with recombination signal binding protein RBP-J kappa, the homologue of Drosophila Suppressor of Hairless.
    EMBO J. 1994 Oct 17;13(20):4973-82 PMID: 7957063
  38. Chromosomal translocations in human cancer.
    Nature. 1994 Nov 10;372(6502):143-9 PMID: 7969446
  39. B-cell proliferation and induction of early G1-regulating proteins by Epstein-Barr virus mutants conditional for EBNA2.
    EMBO J. 1995 Jan 3;14(1):88-96 PMID: 7828599
  40. Transfection of the c-myc oncogene into normal Epstein-Barr virus-harboring B cells results in new phenotypic and functional features resembling those of Burkitt lymphoma cells and normal centroblasts.
    J Exp Med. 1995 Feb 1;181(2):699-711 PMID: 7836923
  41. Regulatory elements in the immunoglobulin kappa locus induce c-myc activation in Burkitt's lymphoma cells.
    Curr Top Microbiol Immunol. 1995;194:415-22 PMID: 7895517
  42. The role of immunoglobulin kappa elements in c-myc activation.
    Oncogene. 1995 Apr 6;10(7):1393-401 PMID: 7731690
  43. A subpopulation of normal B cells latently infected with Epstein-Barr virus resembles Burkitt lymphoma cells in expressing EBNA-1 but not EBNA-2 or LMP1.
    J Virol. 1995 Jun;69(6):3752-8 PMID: 7745723
  44. Inhibition of antigen processing by the internal repeat region of the Epstein-Barr virus nuclear antigen-1.
    Nature. 1995 Jun 22;375(6533):685-8 PMID: 7540727
  45. Identification of a novel promoter located within the Bam HI Q region of the Epstein-Barr virus genome for the EBNA 1 gene.
    DNA Cell Biol. 1995 Sep;14(9):767-76 PMID: 7669254
  46. Redefining the Epstein-Barr virus-encoded nuclear antigen EBNA-1 gene promoter and transcription initiation site in group I Burkitt lymphoma cell lines.
    Proc Natl Acad Sci U S A. 1995 Nov 7;92(23):10565-9 PMID: 7479841
  47. Epstein-Barr virus induction of recombinase-activating genes RAG1 and RAG2.
    J Virol. 1995 Dec;69(12):8155-8 PMID: 7494341
  48. Epstein-Barr virus nuclear antigen 2 (EBNA2)-oestrogen receptor fusion proteins complement the EBNA2-deficient Epstein-Barr virus strain P3HR1 in transformation of primary B cells but suppress growth of human B cell lymphoma lines.
    J Gen Virol. 1996 Feb;77 ( Pt 2 ):227-37 PMID: 8627226
  49. c-myc expression is activated by the immunoglobulin kappa-enhancers from a distance of at least 30 kb but not by elements located within 50 kb of the unaltered c-myc locus in vivo.
    Oncogene. 1996 Mar 21;12(6):1299-307 PMID: 8649832
  50. A vector that replicates as a plasmid and can be efficiently selected in B-lymphoblasts transformed by Epstein-Barr virus.
    Mol Cell Biol. 1985 Feb;5(2):410-3 PMID: 2983194
  51. Influence of Burkitt's lymphoma and primary B cells on latent gene expression by the nonimmortalizing P3J-HR-1 strain of Epstein-Barr virus.
    J Virol. 1989 Apr;63(4):1531-9 PMID: 2538644
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
1996-09-17
Pages
10411-6
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC38398
Subset
IM
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